Behavioral Ecology Vol. 10 No. 2: 128–135 Aerodynamic costs of long tails in male barn swallows Hirundo rustica and the evolution of sexual size dimorphism Andrés Barbosa and Anders Pape Møller Laboratoire d’Ecologie, Université Pierre et Marie Curie, CNRS-URA 258, Bât A, 7e étage, 7, quai Saint Bernard, Case 237, F-75252 Paris, Cedex 05, France Exaggerated tail feathers of birds constitute a standard example of evolution of extravagant characters due to sexual selection. Such secondary sexual traits are assumed to be costly to produce and maintain, and they usually are accompanied by morphological adaptations that tend to reduce their costs. The aerodynamic costs for male barn swallows Hirundo rustica of having long tails were quantified using aerodynamics theory applied to morphological data from seven European populations. Latitudinal differences in tail length were positively correlated with differences in flight costs predicted by aerodynamics theory. A positive relationship between aerodynamic costs of long tails and the degree of sexual size dimorphism was found among populations. Latitudinal differences in foraging costs may result in tail length being relatively similar in males and females in southern populations, whereas the low foraging costs for males in northern populations may allow them to cope with higher aerodynamic costs, giving rise to large sexual size dimorphism. Enlargement of wingspan in males can alleviate but not eliminate the costs of tail exaggeration, and therefore differences in aerodynamic costs of male ornaments were maintained among populations. Sexual size dimorphism in the barn swallow arises as a consequence of latitudinal differences in the advantages of sexual selection for males and the costs of long tails for males and females. Key words: clinal variation, flight costs, sexual selection, tail shape. [Behav Ecol 10:128–135 (1999)] S econdary sexual characters are more exaggerated than homologous characters in closely related species due to the effects of sexual selection and its two main components, male–male competition and female choice (Darwin, 1871). Sexual selection arises because individuals of the chosen sex experience advantages over others of the same species and sex in relation to reproduction. Two different categories of sexual selection models may account for exaggeration of male traits. The Fisherian model of mate choice suggests that female preferences coevolve with the male trait, resulting in the production of exaggerated, attractive, and costly secondary sex traits (Fisher, 1930). At evolutionary equilibrium this cost of the secondary sexual character is balanced by its advantages in terms of increased mating success (Fisher, 1930; Kirkpatrick, 1982; Lande, 1981; Pomiankowski et al., 1991; Sutherland and de Jong, 1991). Alternatively, handicap models assume that the level of signaling adopted by a male is an outcome of individual optimization. Low-quality individuals will be unable to produce a larger sex trait because the cost of such a trait is relatively greater for low- than for high-quality individuals (Andersson, 1986; Grafen, 1990; Heywood, 1989; Iwasa et al., 1991; Kodric-Brown and Brown, 1984; Price et al., 1993; Zahavi, 1975). Thus all these models of sexual selection assume that higher levels of display are prevented because of the costs of signaling. Feather ornaments in birds, and particularly extravagant tails, are standard examples of exaggerated traits that are maintained by sexual selection. Several experimental studies of birds demonstrate that males with long tails experience a Address correspondence to A. Barbosa, who is now at the Departamento de Ecologı́a Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, C/José Gutierrez Abascal, 2, 28006 Madrid, Spain. E-mail: [email protected]. Received 23 October 1997; revised 29 June 1998; accepted 5 July 1998. q 1999 International Society for Behavioral Ecology mating advantage (e.g., Andersson, 1982, 1992; Evans and Hatchwell, 1992; Møller, 1988) at a viability cost (Evans and Thomas, 1992; Møller, 1989; Møller and de Lope, 1994; Møller et al., 1995b; Saino and Møller, 1996; Saino et al., 1997) and support the hypothesis that sexual selection is the mechanism responsible for the evolution of long tails (Møller et al., 1998). Tails of birds are functional units that are shaped by both natural and sexual selection. Aerodynamics theory suggests that only the proximal part of the tail until the point of maximum continuous width is aerodynamically functional and that any area beyond this point does not increase lift, but increases drag (Thomas, 1993). Drag is proportional to the area beyond this point of maximum continuous width, and such tail drag contributes significantly to the parasite drag of the bird (Evans and Thomas, 1992; Thomas and Balmford, 1995), which can cause an increase in the power required for flight (Norberg, 1995). In a forked tail such as that of the barn swallow Hirundo rustica, the maximum lift for any given drag is produced by a spread, triangular tail. The optimum tail shape is one with the outermost tail feathers just slightly more than twice the length of the central feathers when the spread tail just exceeds 1208 (Thomas and Balmford, 1995). An increase in tail length exceeding the optimum ratio of two would increase tail drag and the power of flight and therefore increase the cost of flight. Recently, Norberg (1994) suggested a mechanism that would improve maneuverability by increasing lift and reducing drag. Basically, tail streamers through aeroelastic properties of distal parts of the feather cause a rotation in their sockets, deflecting the leading edge and acting like certain high lift devices in aircraft (Norberg, 1994). Evans and Thomas (1997) predicted from a theoretical study a decrease in turning radius when Norberg’s mechanism was operating. Hence they suggested that the outermost feathers would not be costly but would actually confer a natural selection advantage to males with long streamers. This claim cannot be easily tested because certain parts of Norberg’s hypothesized mechanism Barbosa and Møller • Aerodynamic costs and sexual size dimorphism are difficult to evaluate and relate to improved flight. For example, there is no quantification of the relationship between the degree of the deflecting leading edge mechanism and the length of the tail streamer. Obviously, a certain streamer length causes torsion of the feather, but this torsion could also be produced by a short streamer, as in females or short-tailed males. In fact, Norberg (1994) assumed such a possibility, and although he proposed possible differences in feather characteristics such as flexural stiffness, feather shaft curvature, and torsional rigidity in relation to the length of the streamer, the consequences of such differences remain to be demonstrated. Therefore, the mechanism described by Norberg (1994) does not make any explicit predictions about the cost of a long tail. However, there are several pieces of evidence suggesting that the Norberg effect can be considered a constant acting on the whole range of tail lengths in barn swallows (Barbosa and Møller, in press; Møller et al., 1998). A discussion of the effects of the Norberg mechanism in barn swallows can be found in Møller et al. (1998) and Barbosa and Møller (in press) and in the Discussion of the present paper. Costs of secondary sexual characters can be reduced by the presence of cost-reducing traits (Møller, 1996). For birds with elongated tails, elongation and enlargement of wings and narrowing of the outermost tail feathers have been demonstrated to act as cost-reducing traits (Andersson and Andersson, 1994; Balmford et al., 1994, Møller et al., 1995a). Although geographical variation in sexual size dimorphism in tail length and foraging costs have been reported for the barn swallow (Møller, 1995; Møller and de Lope, 1994; Møller et al., 1995b), aerodynamical costs sensu stricto of long tails remain to be quantified. In this study, we calculated the aerodynamic costs of long tails in male barn swallows from seven European populations. We used a theoretical framework to study the relationship between such costs and the degree of sexual dimorphism in tail length and the size of cost-reducing characters along a latitudinal gradient in size dimorphism. If long streamers in male barn swallows have evolved by sexual selection, we predicted a significant positive relationship between costs of long tails and sexual size dimorphism. METHODS Barn swallows are small (approximately 20 g), monogamous, semicolonial passerine birds that feed on insects caught on the wing. Sexual size dimorphism is slight with the exception of the outermost feathers of the forked tail. Male tail length is only weakly correlated with structural body size, and individual males are highly consistent in tail length among years (Møller, 1991). Male barn swallows attempt to attract a mate by performing displays of their tail ornaments in flight or while perched (Møller, 1988). Female barn swallows visit several males before making their mate choice, and males with long and symmetrical tails are preferred over ones with short and asymmetrical tails (Møller, 1988, 1990, 1992a, 1994). Long-tailed males also experience a number of other sexual selection advantages (Møller, 1990, 1992b, 1994). Nestlings are fed by both parents for an average of 3 weeks before fledging. The studies took place at seven different sites. Kraghede, Denmark (578 N, 108 E) is an open farmland site with scattered plantations, ponds, and hedgerows. The barn swallows usually breed on farms either solitarily or in colonies of up to 50 pairs. A detailed description of the population is given in Møller (1994). Two study sites in the Ukraine were situated on large cooperative farms in open farmland habitat near Chernobyl (528 N, 298 E) and Kanev (508 N, 318 E), separated by a distance of 300 km. The main crops were grass and wheat. 129 Figure 1 Study site cladogram built from differences in latitudinal coordinates and the increased percentage drag and flight power at each locality when comparing males with an optimal tail shape and mean tail length of males. The barn swallows breed inside stables and cowsheds. The number of breeding pairs per colony ranged from 20 to 120 pairs. Pärnu, Estonia (588 N, 248 E), is a mixed farmland and forest habitat with solitary pairs or colonies of up to 50 pairs of swallows breeding inside stables. The study site at Tiszatelek, Hungary (488 N, 218 E), is an open farmland habitat with breeding sites at farms having single pairs up to more than 25 pairs. The study site at Milano, Italy (458 N, 98 E), is an open farmland area. The main crops are maize, grass, wheat, and soybeans. Fields are bordered by hedges and trees. Barn swallows breed mainly in cowsheds, milking rooms, garages, and sometimes outdoors. The number of nests in the colonies ranged from 18 to 59. The Badajoz, Spain (398 N, 78 W), study site consists of open farmland with scattered groups of trees around farms and rivers. The main crops are grass, maize, and wheat. Barn swallows breed solitarily or colonially (up to 50 pairs) in farmhouses and other buildings. The distance between study sites and the nearest neighboring site was on average 908 km (SE 5 160, range 300–1500 km, n 5 7). The average natal dispersal of barn swallows is known to be 0.7 km for males and 2.5 km for females based on ringing recoveries (Cramp, 1988), and other estimates are of a similar magnitude (Glutz von Blotzheim and Bauer, 1985). Breeding dispersal is also restricted and rarely exceeds 1 km (Cramp, 1988; Glutz von Blotzheim and Bauer, 1985). This means that the average distance between study sites is several hundred times the average natal dispersal distance. Gene flow between study sites should therefore be minimal (Endler, 1977; Slatkin, 1985). The statistical dependence of data from different populations is likely to be related to geographical proximity, and this may affect the reliability of statistical analyses in a similar way to phylogenetic analyses (Felsenstein, 1985). To avoid this problem, we adopted the independent contrast method using geographical distance as an estimate of genetic divergence between populations based on an assumption of isolation by distance. As geographic variation in most morphological traits of the barn swallow shows a latitudinal cline (Møller, 1995), we built a cladogram based on latitudinal coordinates of each study site (Figure 1), using the unweighted pair-group average method (UPGM; James and McCulloch, 1990; Sneath and Sokal, 1973). Statistical analyses of relations between characters were determined using contrasts derived from the geographical distance cladogram. These contrasts were calculated as the value of a trait (e.g., tail dimorphism) in one population (or node) of the clado- Behavioral Ecology Vol. 10 No. 2 130 Table 1 Morphological measurements of males of different barn swallows populations (means 6 SE) Population Wing span (mm) Badajoz Milano Tiszatelek Kanev Chernobyl Kraghede Pärnu 321.73 322.03 335.07 324.59 330.74 329.10 328.71 6 6 6 6 6 6 6 0.83 0.44 0.91 0.39 0.82 0.03 3.03 Tail length (mm) 97.86 104.48 112.18 109.75 107.68 107.48 110.36 6 6 6 6 6 6 6 1.39 0.58 1.43 0.99 1.45 0.30 1.43 gram subtracted from the value of the closest population (or node). Thus each population or node was compared to its closest population. Euclidean distances were used as branch lengths in contrast analyses because Felsenstein’s method requires knowledge of branch lengths in the cladogram (see Felsenstein, 1985, for more details). To be able to identify covariation between variables, regression through the origin was used to test the relationship (Garland et al., 1992). To make unique representations of bivariate scatterplots, one must set all contrasts for one trait (e.g., the independent variable) positive, while switching signs for the other trait’s corresponding contrasts. Regression through the origin yields the same results whether contrasts are thus positivized (Garland et al., 1992). Most adult barn swallows were captured in mist nets at the breeding sites. All birds were provided with a numbered aluminium band to allow identification. Individuals were sexed from the presence (females) or absence (males) of a brood patch and by the shape of the cloacal protuberance (Svensson, 1984). Morphological characters (Table 1) were measured by A.P.M. (Kraghede, Pärnu, Chernobyl, Kanev) or using exactly the same methods by other field workers given instructions by A.P.M. in order to reduce interobserver variability. However, we included the person who took the measurements as a dummy variable (0 for other persons, 1 for A.P.M.) to test whether interobserver variability had affected the results. The morphological characters were used as dependent variables in multiple linear regression analyses with latitude, the person dummy variable, and the latitude-person variable interaction as independent variables. None of the regression coefficients for the dummy variable or the interaction were statistically significant (p . .05), which suggests that variation in morphology along the latitudinal gradient was unbiased by the person who had taken the measurements. The length of the outermost tail feathers, hereafter called tail length, and the central tail feathers were measured with a ruler to the nearest millimeter. We measured wing span to the nearest millimeter as the distance between wing tips when the wings were stretched maximally. Body mass was recorded to the nearest 0.1 g using a Pesola spring balance. We determined sexual size dimorphism in tail length as the residuals from a regression of mean values for males regressed on mean values for females in each population. The regression was statistically highly significant and positive [male tail length 5 51 1 0.36 (female tail length), F 5 18.57, df 5 1,5, r 5 .88, p 5 .007]. To calculate tail drag and power curves of power consumption in each population, we used the mean tail length and the hypothetical optimum tail length for each population in the aerodynamic models (tail length divided by central feather length equaling two; Thomas and Balmford, 1995). The tail was assumed to have a triangular shape with streamers in Central tail length (mm) Body mass (g) 42.76 44.89 47.83 44.08 44.68 44.31 43.12 6 6 6 6 6 6 6 0.18 0.11 0.24 0.24 0.35 0.008 0.27 18.44 18.52 19.46 18.30 18.63 19.14 19.03 6 6 6 6 6 6 6 0.17 0.09 0.13 0.12 0.18 0.04 0.18 Sample size 55 212 54 69 50 856 41 the former case and a triangular tail without streamers projecting beyond the maximum continuous span in the latter case. The Norberg effect has been considered constant because there is no empirical evidence of differential effects among different individuals (Barbosa and Møller, in press; Møller et al., 1998; see also Norberg, 1994). Tail drag calculations were performed using the formula from Prandtl and Tietjens (1934) for a flat plate with Reynolds number less than 106 (Evans and Thomas, 1992) Drag 5 0.6635rsÏlvu3 where r 5 1.23 (kg/m3) is the density of air, s is tail span, l is tail length, v 5 1.45 3 1025 (m2s21) is the kinematic viscosity of air, and u is velocity. Power curves of power consumption were calculated using a modified version of the computer programs in Pennycuick (1989) adding tail drag. We used Pennycuick’s model because it provides the most realistic estimate of flight costs in comparison with other aerodynamic models (Welham, 1994; see also Evans and Thomas, 1992). This model allows calculations of aerodynamic performance in relation to flight speed on the basis of body mass and wingspan of birds (Pennycuick, 1989). Increases in power consumption and drag due to tail length in each population were calculated as the percentage increase for the mean tail length with respect to the hypothetical optimum tail length (see above). The increase in wingspan needed to compensate for the flight costs due to tail elongation were calculated. Wingspan values were manipulated in the computer models until flight costs at the mean speed considered for a bird with an elongated tail were the same as for a bird with the optimal tail length. Latitudinal variation in tail length has been related to latitudinal variation in foraging costs (Møller et al., 1995a). We have explored the possible variation in such a foraging costs comparing the size of prey available for barn swallows with the size of prey captured by barn swallows at different latitudes. We have compared the percentage increase of mean size between available prey and selected prey in the three populations for which this kind of data were available (Kraghede, 578 N, Møller AP, unpublished data; Stirling, 568, Turner, 1980; Lippstadt, 518, Loske, 1993). RESULTS Table 2 shows differences in drag at different flight speeds between optimal and elongated tails in the seven populations of barn swallows. Assuming a mean flight speed of barn swallows to be about 10 m/s (Harrison, 1931; Meinertzhagen, 1955), the percentage increase of drag in males with a long tail in relation to the hypothetical optimum tail length ranged from 7.0% in the Badajoz population to 15.3% in the Pärnu population (Figure 1). The effect of increase in drag due to Barbosa and Møller • Aerodynamic costs and sexual size dimorphism 131 Table 2 Calculated drag (1023 Newton) from aerodynamics theory of the optimum (Opt) tail length (see Methods) and of mean tail length in male barn swallows from seven European populations Air speed (m/s) Opt Mean Opt 3 4 5 6 7 8 9 10 0.6999 1.0776 1.5061 1.9798 2.4948 3.0481 3.6372 4.2599 0.7487 1.1528 1.6111 2.1178 2.6688 3.2606 3.8907 4.5569 0.7526 1.1587 1.6193 2.1286 2.6824 3.2773 3.9106 4.5801 Badajoz Milano Tiszatelek Kanev Mean Opt Mean Opt 0.8122 1.2505 1.7476 2.2973 2.8950 3.5370 4.2205 4.9431 0.8275 1.2741 1.7806 2.3407 2.9497 3.6038 4.3002 5.0365 0.8962 1.3797 1.9283 2.5348 3.1942 3.9026 4.6567 5.4541 0.7326 1.1279 1.5763 2.0721 2.6112 3.1903 3.8068 4.4586 long tails relative to the optimal tail length on power of flight is shown in Table 3. At the mean speed considered, the percentage of power increase with respect to the optimum tail length ranged from 0.9% in the Badajoz population to 1.5% in the Kanev population (Figure 1). Mean percentage of drag and flight power increase between optimal and long-tailed phenotypes was 10.2% and 1.3%, respectively. The results did not change using the independent contrast method instead of the species regression which considers each population to contribute a statistically independent data point. However, we present the results for the independent contrast method to correct for any possible effects of independence due to geographical proximity. The increase in tail drag and flight power were significantly positively related to sexual size dimorphism in the seven populations [b (SE) 5 0.84 (0.24), t 5 3.47, df 5 5, p 5 .01; b (SE)5 0.80 (0.26), t 5 3.01, df 5 5, p 5 .02; Figure 2). The percentage increase in wingspan was positively, but not significantly, related to the percentage increase in tail elongation [b 5 0.72 (0.30), t 5 2.34, df 5 5, p 5 .06; Figure 3]. Table 4 shows the percentage difference in mean prey size captured relative to the available prey in the three populations. Northern populations selected much larger prey with respect to the size available than southern populations, consistent with a decrease in foraging costs toward the north. DISCUSSION Exaggeration of secondary sexual characters such as tail feathers is costly according to current models of sexual selection (Andersson, 1986; Fisher, 1930; Grafen, 1990; Heywood, 1989; Iwasa et al., 1991; Pomiankowski et al., 1991; Zahavi, 1975). A Chernobyl Kraghede Pärnu Mean Opt Mean Opt Mean Opt Mean 0.8174 1.2585 1.7588 2.3120 2.9135 3.5596 4.2475 4.9747 0.7476 1.1510 1.6085 2.1145 2.6646 3.2555 3.8846 4.5497 0.8206 1.2588 1.7657 2.3211 2.9250 3.5737 4.2642 4.9944 0.7383 1.1367 1.5886 2.0883 2.6316 3.2152 3.8365 4.4934 0.8131 1.2518 1.7495 2.2998 2.8991 3.5408 4.2251 4.9484 0.7085 1.0908 1.5245 2.0040 2.5753 3.0853 3.6815 4.3119 0.8015 1.2339 1.7245 2.2689 2.8567 3.4902 4.1647 4.8777 number of different costs of elongated tails have been reported. Møller (1989) and Møller and de Lope (1994) provided experimental evidence for the presence of a considerable viability cost of long tails in male barn swallows. Longtailed males were better able to survive tail elongation, whereas short-tailed males survived relatively better when their tails were shortened. Foraging costs of tail exaggeration have also been reported in barn swallows (Møller, 1989; Møller and de Lope, 1994; Møller et al., 1995a): males with experimentally elongated tails captured more and smaller prey than tail-shortened individuals, but males with naturally long tails were less affected by experimental treatment. Optimal prey for the barn swallow are large, actively flying insects according to optimal foraging models (Bryant and Turner, 1982; Turner, 1982), but these prey are difficult to catch for long-tailed males, both with naturally and experimentally elongated tails (Møller, 1992b; de Lope and Møller, 1993; Møller et al., 1995a). Direct aerodynamic costs of long tails have been demonstrated a few times. Evans and Thomas (1992) showed that malachite sunbirds (Nectarinia johnstoni) with experimentally elongated tails spent less time flying than before manipulation. The theoretical aerodynamic effects of tail elongation have been analyzed for bird species with different tail morphologies (Balmford et al., 1993; Norberg, 1995; Thomas, 1993; Thomas and Balmford, 1995). Here we calculated the aerodynamic costs (in terms of increased drag and flight power) of tail elongation in male barn swallows from seven European populations and investigated how such costs were related to sexual size dimorphism, geographical variation in dimorphism, and the presence of cost-reducing morphological traits. Table 3 Calculated flight power (W) from aerodynamics theory for the optimum (Opt) tail length (see Materials and Methods) and mean tail length in male barn swallows from seven European populations Air speed (m/s) Badajoz Opt Mean Opt 3 4 5 6 7 8 9 10 0.206 0.196 0.198 0.209 0.229 0.258 0.297 0.346 0.206 0.196 0.198 0.210 0.230 0.259 0.299 0.349 0.207 0.197 0.199 0.211 0.231 0.261 0.300 0.350 Milano Tiszatelek Kanev Mean Opt Mean Opt 0.207 0.198 0.200 0.212 0.232 0.263 0.303 0.354 0.213 0.203 0.205 0.217 0.239 0.270 0.311 0.364 0.213 0.203 0.206 0.219 0.241 0.272 0.315 0.433 0.201 0.192 0.194 0.206 0.226 0.255 0.294 0.344 Chernobyl Kraghede Pärnu Mean Opt Mean Opt Mean Opt Mean 0.202 0.193 0.195 0.207 0.228 0.258 0.298 0.349 0.202 0.193 0.195 0.207 0.228 0.258 0.297 0.347 0.202 0.193 0.196 0.208 0.230 0.260 0.301 0.352 0.212 0.202 0.203 0.215 0.236 0.265 0.305 0.356 0.212 0.202 0.204 0.216 0.237 0.268 0.309 0.361 0.210 0.200 0.202 0.213 0.233 0.263 0.303 0.353 0.211 0.201 0.203 0.215 0.236 0.266 0.307 0.358 Behavioral Ecology Vol. 10 No. 2 132 Figure 3 Relationship between contrasts of male tail length and contrasts of theoretical wingspan increase to reduce flight costs. Figure 2 Relationships between (A) contrasts of increase in drag and contrasts of flight power and (B) contrasts of sexual size dimorphism among barn swallow populations. The optimal tail shape for an aerially foraging bird with a forked tail that gives rise to the maximum lift-to-drag ratio is one that forms a triangular platform and a straight trailing edge when the tail is spread at an angle of approximately 1208 (Thomas, 1993). The outermost tail feathers will then be twice the length of the central tail feathers. Male barn swallows in all seven populations had outermost tail feathers that on average were much longer than twice the length of the central tail feathers (see also Møller, 1995; Møller et al., 1995b). Such elongation increases costs because any area beyond the point of maximum continuous width of the tail does not increase lift but increases drag (Thomas, 1993). Overcoming drag is the major energetic cost of flight (Gill and Wolf, 1975). Energy expenditure on locomotion cannot be used for other demanding activities such as an efficient immune system, and the energy cost of ornament exaggeration thus imposes a reduction in the amount of resources available for immune function (König and Schmid-Hempel, 1995; Saino and Møller, 1996). Flight costs are affected by the different degree of tail elongation of males in different populations of barn swallows (Tables 2 and 3), increasing with latitude (Figure 1). Tail length manipulation affects flight costs and foraging efficiency, which may give rise to the observed reduced survival of male barn swallows with experimentally elongated tails and the increased survival of males with shortened tails (Møller, 1989; Møller and de Lope, 1994). The cost of barn swallow tail ornaments may vary geographically if ambient temperature affects insect physiology and thereby the energy cost of prey capture. Flight performance of insects, including their ability to escape avian predators, depends on ambient temperature (Beament and Treherne, 1968; Taylor, 1963; Wigglesworth, 1972). Barn swallows are specialist predators of large, actively flying Diptera that constitute the optimal diet (Bryant and Turner, 1982). Large insects are more difficult to catch at the higher temperatures that predominate at southern latitudes, as shown by Møller et al. (1995a). Geographic variation in the mean size of insect prey captured by barn swallows relative to the mean size available is consistent with a latitudinal trend in foraging costs (Table 4). Although foraging costs decrease with increasing insect abundance due to a reduction in the cost of searching for a new prey, the cost of prey capture per item will be unaffected by prey abundance. Prey-searching flight does not require the same maneuverability and agility as that of prey capture because it consists of rapid flight with the tail furled and therefore has little aerodynamic cost (Thomas, 1996). Our aerodynamic analyses are thus consistent with an eco- Table 4 Mean size of available insect prey and mean size of prey captured by adult barn swallow in three different populations a Population Mean size of available prey Mean size of taken prey % Size increase between available and captured prey Kraghede (578 N) Stirling (568 N) Lippstadt (518 N) 4.8 mm 2.21 g 3.6 mm 10.6 mm 6.61 g 4.8 mm 120 44a 33 The percentage increase for Stirling was calculated based on the cube-root of the mass of insects. Barbosa and Møller • Aerodynamic costs and sexual size dimorphism 133 morphological relationship between aerodynamic costs due to tail elongation and the difficulty of capturing insects. The lowest flight costs are found in southern populations in which foraging costs are the highest due to superior insect flight performance. Aerodynamic costs increase with latitude and are the highest in populations where insects can readily be caught. Therefore, there appears to be a trade-off between foraging costs and aerodynamic costs affecting the size of tail ornaments in male barn swallows. Geographic variation in sexual size dimorphism in barn swallows has been explained by geographic variation in the costs of long tails for the two sexes (Møller, 1995). We found a positive relationship between aerodynamic costs of long tails and the degree of sexual size dimorphism among populations (Figure 2), suggesting that long tails in males have evolved by sexual selection. As shown above, aerodynamic costs during foraging enforce the tail morphology of males at southern latitudes to be close to the aerodynamic optimum and therefore close to the morphology of female tails. At high latitudes, where foraging costs are low, males are less constrained, and they can cope with higher aerodynamic costs, and larger differences in sexual size dimorphism thus evolve (see also Møller, 1995). Our previous arguments have only considered males. However, the evolution of sexual size dimorphism is a process governed by the differential effects of natural and sexual selection on individuals of the two sexes. Although there is a slight latitudinal increase in tail length in females, this is considerably less than the increase in males (Møller, 1995), presumably because long tails are more costly for females than for males. Tail elongation in females has been suggested to be a consequence of a correlated response to sexual selection on males (Cuervo et al., 1996) because of a strong positive genetic correlation between the sexes (Møller, 1993). Thus geographic variation in sexual size dimorphism in the barn swallow seems to arise as a consequence of foraging costs of long tails in both sexes, allowing little divergence at southern latitudes, but more divergence in cold climates, where large dipteran prey are relatively easily captured even by long-tailed males. Recently, Norberg (1994) proposed a hypothetical mechanism for increasing lift by the barn swallow tail due to the distal feather bending upward and backward with the torsion of the feather deflecting the leading edge. This mechanism was suggested to provide an explanation based on natural selection for the evolution of tail streamers in the barn swallow (Evans and Thomas, 1997; Norberg, 1994; Thomas and Rowe, 1997). Norberg’s paper only describes a possible mechanism that relates feather bending and feather torsion to increased lift. Norberg does not present data demonstrating that such relationships are dependent on tail length. The functional relationship between streamer length and the degree of deflection of the leading edge of the tail remains to be determined. Moreover, differential lift related to different degrees of deflection also remains to be demonstrated. The unknown relationship between the different parameters involved in the Norberg mechanism makes the effect difficult to assess. Aerodynamic calculations can only include Norberg’s mechanism when the relationship between streamer length, the degree of distal feather bending (upward and backward), the degree of feather torsion, and the amount of lift achieved have been quantified. However, several pieces of evidence suggest that the Norberg effect is independent of streamer length and that the mechanism acts for short streamers such as those of female barn swallows or those of species of hirundines with shallow, forked tails (Norberg, 1994). Norberg (1994) assumed that even without streamers, it would be possible to achieve a similar effect to improve flight (see also Møller et al., 1998; Barbosa and Møller, in press). The following evidence suggests that the Norberg mechanism is unrelated to the length of tail feathers. First, differences in the length of streamers of male and female barn swallows are unrelated to differences in the flight costs of each sex (Barbosa et al., submitted). Second, the probability of feather damage is positively correlated with tail length in male barn swallows, increasing the flight costs for long-tailed individuals due to the effects of tail asymmetry on flight performance (Barbosa et al., submitted). Third, there are differences in the evolution of deep and shallow forked tails in hirundines (Barbosa and Møller, unpublished data). Fourth, sexual size dimorphism in juveniles during the first winter cannot be explained by Norberg effect because the outermost tail feathers do not extend beyond the central feathers when the tail is spread at 1208. The ratio of the length of the outermost tail feathers to that of the central feathers is on average 1.55 in juvenile males and 1.47 in juvenile females (Cadée et al., submitted). Therefore, it is unlikely that sexual size dimorphism in juveniles is explained by natural selection through the Norberg effect. Instead, sexual size dimorphism in juveniles could be explained in the light of sexual selection acting on adult dimorphism. Finally, Norberg assumed a relationship between feather traits such as the feather shaft, curvature, and flexion stiffness, but, as stated above, these hypothetical relations remain to be tested. Furthermore, if the Norberg mechanism was dependent on tail length, we should expect streamer length to be related to the functional part of the outermost tail feather. However, we have determined the relationship between streamer length and basal feather length and found no association in either sex in five different populations of barn swallows (Barbosa and Møller, unpublished data). These results also suggest that the deflecting leading edge mechanism is not determined by the relation between basal feather length and streamer length. Several studies have shown that the presence of costly secondary sex traits often results in the evolution of cost-reducing characters (see review in Møller, 1996). Aerodynamic costs due to tail elongation can be reduced by an enlarged wingspan (Thomas, 1993). Birds with exaggerated tail ornaments have longer wings than closely related species without ornaments (Andersson and Andersson, 1994; Balmford et al., 1994). Male barn swallows have reduced the aerodynamic costs of their outermost tail feathers by increased wingspans and a reduced width of the outermost tail feathers (Møller et al., 1995b). Our analyses show that there is a positive, but not significant, relationship between the increase in wing length needed to reduce the flight costs and the degree of sexual size dimorphism among barn swallow populations (Figure 3). However, despite such cost reduction, a flight cost of long tails in males still remains, as indicated by differences in flight costs among populations. In conclusion, long tail streamers of male barn swallows entail aerodynamic costs that are reduced by the presence of cost-reducing characters such as an increased wingspan. Geographical differences in male tail length and their inherent aerodynamic costs are constrained by foraging costs that are responsible for geographic differences in sexual size dimorphism. F. de Lope, N. Saino, M. Kose, and T. Szep kindly helped collecting data. A.P.M. was supported by grants from the Swedish and Danish Natural Science Research Councils. A.B. was supported by a Marie Curie postdoctoral grant of the European Communities (ERB4001GT951093). Anders Hedenström kindly reviewed a first version of the manuscript and made helpful suggestions. T. Garland 134 kindly provided the programs for calculations of independent contrasts. REFERENCES Andersson M, 1982. Female choice selects for extreme tail length in a widowbird. Nature 299:818–820. Andersson M, 1986. Evolution of condition-dependent sex ornaments and mating preferences: Sexual selection based on viability differences. Evolution 40:804–816. Andersson S, 1992. Female preference for long tails in lekking Jackson’s widowbirds: Experimental evidence. Anim Behav 43:379–388. Andersson S, Andersson M, 1994. Tail ornamentation, size dimorphism and wing length in the genus Euplectes (Ploceinae). Auk 111: 80–86. Balmford A, Jones IL, Thomas ALR, 1994. How to compensate for costly sexually selected tails: the origin of sexually dimorphic wings in long-tailed birds. Evolution 48:1062–1070. Balmford A, Thomas ALR, Jones IL, 1993. Aerodynamics and the evolution of long tails in birds. Nature 36:628–630. Barbosa A, Møller AP, in press. Sexual selection and tail streamers in the barn swallow: appropriate test of the function of size-dimorphic long tails. Behav Ecol. Beament JWL, Treherne JE, 1968. Insects and physiology. New York: Elsevier. Bryant DM, Turner K, 1982. Central place foraging by swallows: the question of load size. Anim Behav 30:845–856. Cramp S, 1988. Handbook of the birds of Europe, the Middle East and North Africa, vol. 5. Oxford: Oxford University Press. Cuervo JJ, de Lope F, Møller AP, 1996. The function of long tails in female barn swallows (Hirundo rustica): an experimental study. Behav Ecol 7:132–136. Darwin C, 1871. The descent of man, and selection in relation to sex. London: Murray. de Lope F, Møller AP, 1993. Female reproductive effort depends on the degree of ornamentation of their mates. Evolution 47:1152– 1160. Endler JA, 1977. Geographic variation, speciation, and clines. Princeton, New Jersey: Princeton University Press. Evans M, Hatchwell BJ, 1992. An experimental study of male adornment in the scarlet-tufted malachite sunbird: II The role of the elongated tail in mate choice and experimental evidence for a handicap. Behav Ecol Sociobiol 29:421–427. Evans MR, Thomas ALR, 1992. The aerodynamic and mechanical consequences of elongated tails in the scarlet-tufted malachite sunbird: measuring the cost of a handicap. Anim Behav 43:337–347. Evans MR, Thomas ALR, 1997. Testing the functional significance of tail streamers. Proc R Soc Lond B 264:211–217. Felsenstein J, 1985. Phylogenies and the comparative method. Am Nat 125:1–15. Fisher RA, 1930. The genetical theory of natural selection. Oxford: Clarendon Press. Garland T, Harvey PH, Ives AR, 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32. Gill FB, Wolf LL, 1975. Economics of feeding territoriality in the golden-winged sunbird. Ecology 56:333–345. Glutz von Blotzheim UN, Bauer KM, 1985. Handbuch der Vögel Mitteleuropas, vol 10/I. Wiesbaden: AULA-Verlag. Grafen A, 1990. Sexual selection unhandicapped by the Fisher process. J Theor Biol 144:475–516. Harrison TH, 1931. On the normal flight speeds of birds. Br Birds 25:86–96. Heywood JS, 1989. Sexual selection by the handicap principle. Evolution 43:1387–1397. Iwasa Y, Pomiankowski A, Nee S, 1991. The evolution of costly mate preferences. II. The ‘‘handicap’’ principle. Evolution 45:1431–1442. James FC, McCulloch CE, 1990. Multivariate analysis in ecology and systematics: panacea or Pandora’s box? Annu Rev Ecol Syst 21:129– 166. Kirkpatrick M, 1982. Sexual selection and the evolution of female choice. Evolution 36:1–12. Kodric-Brown A, Brown JH, 1984. Truth in advertising: the kinds of traits favored by sexual selection. Am Nat 124:303–323. Behavioral Ecology Vol. 10 No. 2 König C, Schmid-Hempel P, 1995. Foraging activity and immunocompetence in workers of the bumble bee Bombus terrestris L. Proc R Soc Lond B 260:225–227. Lande R, 1981. Models of speciation by sexual selection on polygenic characters. Proc Natl Acad Sci USA 78:3721–3725. Loske KH, 1993. Untersuchungen zu Überlebensstrategien der Rauchschwalbe (Hirundo rustica) in Brutgebiet (Ph D thesis). Göttingen: Cuvillier Verlag. Meinertzhagen R, 1955. The speed and altitude of bird flight (with notes on other animals). Ibis 97:81–117. Møller AP, 1988. Female choice selects for male sexual tail ornaments in the monogamous swallow. Nature 332:640–642. Møller AP, 1989. Viability costs of male tail ornaments in a swallow. Nature 339:132–135. Møller AP, 1990. Male tail length and female mate choice in the monogamous swallow Hirundo rustica. Anim Behav 39:458–465. Møller AP, 1991. Sexual selection in the monogamous barn swallow (Hirundo rustica). I. Determinants of tail ornament size. Evolution 45:1823–1836. Møller AP, 1992a. Female swallow preference for symmetrical male sexual ornaments? Nature 357:238–240. Møller AP, 1992b. Sexual selection in the monogamous swallow (Hirundo rustica). II. Mechanisms of intersexual selection. J Evol Biol 5:603–624. Møller AP, 1993. Sexual selection in the barn swallow (Hirundo rustica). III. Female tail ornaments. Evolution 47:417–431. Møller AP, 1994. Sexual selection and the barn swallow. Oxford: Oxford University Press. Møller AP, 1995. Sexual selection in the barn swallow (Hirundo rustica). V. Geographic variation in ornament size. J Evol Biol 8:3–19. Møller AP, 1996. The cost of secondary sexual characters and the evolution of cost-reducing traits. Ibis 138:112–119. Møller AP, Barbosa A, Cuervo JJ, de Lope F, Merino S, Saino N, 1998. Sexual selection and tail streamers in the barn swallow. Proc R Soc Lond B 265:409–414. Møller AP, de Lope F, 1994. Differential costs of a secondary sexual character: an experimental test of the handicap principle. Evolution 48:1676–1683. Møller AP, de Lope F, López Caballero JM, 1995a. Foraging costs of a tail ornament: experimental evidence from two populations of barn swallows Hirundo rustica with different degrees of sexual size dimorphism. Behav Ecol Sociobiol 37:289–295. Møller AP, de Lope F, Saino N, 1995b. Sexual selection in the barn swallow Hirundo rustica. VI. Aerodynamic adaptations. J Evol Biol 8:671–687. Norberg RA, 1994. Swallow tail streamer is a mechanical device for self-deflection of tail leading edge, enhancing aerodynamic efficiency and flight manoeuvrability. Proc R Soc Lond B 257:227–233. Norberg UM, 1995. How a long tail and changes in mass and wing shape affect the cost for flight in animals. Funct Ecol 9:48–54. Pennycuick CJ, 1989. Bird flight performance: A practical calculation manual. Oxford: Oxford University Press. Pomiankowski A, Iwasa, Nee S, 1991. The evolution of costly mate preferences. I. Fisher and biased mutation. Evolution 45:1422– 1430. Prandtl L, Tietjens OG, 1934. Applied hydro- and aerodynamics. New York: Dover Publications. Price T, Schluter D, Heckman NE, 1993. Sexual selection when the female directly benefits. Biol J Linn Soc 48:187–211. Saino N, Cuervo JJ, Krivacek M, de Lope F, Møller AP, 1997. Experimental manipulation of tail ornament size affects haematocrit of male barn swallows, Hirundo rustica. Oecologia 110:186–190. Saino N, Møller AP, 1996. Sexual ornamentation and immunocompetence in the barn swallow. Behav Ecol 7:227–232. Slatkin M, 1985. Gene flow in natural populations. Annu Rev Ecol Syst 16:393–340. Sneath PHA, Sokal RR, 1973. Numerical taxonomy, the principles and practice of numerical classification. San Francisco: WH Freeman. Sutherland WJ, de Jong MCM, 1991. The evolutionarily stable strategy for secondary sexual characters. Behav Ecol 2:16–20. Svensson L, 1984. Identification guide to European passerines. Stockholm: L. Svensson. Taylor LR, 1963. Analysis of the effect of temperature on insects in flight. J Anim Ecol 32:99–117. Barbosa and Møller • Aerodynamic costs and sexual size dimorphism 135 Thomas ALR, 1993. On the aerodynamics of birds’ tails. Phil Trans R Soc Lond B 340:361–380. Thomas ALR, 1996. The flight of birds that have wings and a tail: variable geometry expands the envelope of flight performance. J Theor Biol 183:237–245. Thomas ALR, Balmford A, 1995. How natural selection shapes birds’s tails. Am Nat 146:848–868. Thomas ALR, Rowe L, 1997. Experimental tests on tail elongation and sexual selection in swallows (Hirundo rustica) do not affect the tail streamer and cannot test its function. Behav Ecol 8:580– 581. Turner AK, 1980. The use of time and energy by aerial feeding birds (PhD thesis). Stirling, UK: University of Stirling. Turner AK, 1982. Optimal foraging by the swallow: prey size selection. Anim Behav 30:862–872. Welham CVJ, 1994. Flight speeds of migrating birds: a test of maximum range speed predictions from three aerodynamic equations. Behav Ecol 5:1–8. Wigglesworth VB, 1972. The principles of insect physiology, 7th ed. London: Chapman and Hall. Zahavi A, 1975. Mate selection—a selection for a handicap. J Theor Biol 53:205–214.
© Copyright 2024 Paperzz